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(Diptera: Culicidae) Based on Antennal Sensilla of Adult Females

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(Diptera: Culicidae) Based on Antennal Sensilla of Adult Females Tropical Biomedicine 36(4): 926–937 (2019) A method for distinguishing the important malaria vectors Anopheles dirus and An. cracens (Diptera: Culicidae) based on antennal sensilla of adult females Taai, K.1, Harbach, R.E.2, Somboon, P.3, Sriwichai, P.4, Aupalee, K.3, Srisuka, W.5, Yasanga, T.6, Phuackchantuck, R.7, Jatuwattana, W.3, Pusawang, K.3 and Saeung, A.3* 1Faculty of Veterinary Medicine, Western University, Kanchanaburi 71170, Thailand 2Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK 3Center of Insect Vector Study, Department of Parasitology, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand 4Department of Medical Entomology, Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand 5Entomology Section, Queen Sirikit Botanic Garden, Chiang Mai 50180, Thailand 6Medical Science Research Equipment Center, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand 7Research Administration Sections, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand *Corresponding author e-mail: [email protected] Received 25 February 2019; received in revised form 26 June 2019; accepted 28 June 2019 Abstract. Some species of the Anopheles dirus species complex are considered to be highly competent malaria vectors in Southeast Asia. Anopheles dirus is the primary vector of Plasmodium falciparum and P. vivax while An. cracens is the main vector of P. knowlesi. However, these two species are difficult to distinguish and identify based on morphological characters. Hence, the aim of this study was to investigate the potential use of antennal sensilla to distinguish them. Large sensilla coeloconica borne on the antennae of adult females were counted under a compound light microscope and the different types of antennal sensilla were examined in a scanning electron microscope. The antennae of both species bear five types of sensilla: ampullacea, basiconica, chaetica, coeloconica and trichodea. Observations revealed that the mean numbers of large sensilla coeloconica on antennal flagellomeres 2, 3, 7, 10 and 12 on both antennae of both species were significantly different. This study is the first to describe the types of antennal sensilla and to discover the usefulness of the large coeloconic sensilla for distinguishing the two species. The discovery provides a simple, reliable and inexpensive method for distinguishing them. INTRODUCTION to eliminate malaria by 2020. In Thailand, the total number of confirmed malaria cases in Malaria is a disease caused by plasmodial 2016 was 37,209 (Bureau of Vector Borne parasites that are transmitted to humans Diseases, Ministry of Public Health, 2017). through the bites of female Anopheles Seven taxonomic groups are known to mosquitoes. There were approximately 219 include the main malaria vectors in Southeast million malaria cases in 90 countries and an Asia, i.e. the Culicifacies, Dirus, Fluviatilis, estimated 435,000 deaths due to the disease Leucosphyrus, Minimus and Sundaicus in 2017 (WHO, 2018). For example, 1,398 Complexes, and the Maculatus Group cases of falciparum malaria were reported (Manguin et al., 2008). According to Sallum in 28 provinces of China in 2011, especially et al. (2005), the Dirus Complex comprises in epidemic areas of Yunnan and Hainan seven species: An. baimaii Sallum & provinces (WHO, 2018). China is now aiming Peyton, An. cracens Sallum & Peyton, An. 926 dirus Peyton & Harrison, An. elegans James, MATERIALS AND METHODS An. nemophilous Peyton & Ramalingam, An. scanloni Sallum & Peyton and An. Mosquitoes and species identification takasagoensis Morishita. Takano et al. (2010) Specimens of laboratory strains of An. dirus added an eighth species, informally denoted were originally collected in Mae Sod District, as “aff. takasagoensis”. Anopheles dirus has Tak Province, Thailand. Specimens of free- a wide distribution in eastern Asia, being mating An. cracens were originally from recorded in Cambodia, China (Yunnan the Armed Forces Research Institute of Province and Hainan Island), Laos, Myanmar, Medical Sciences laboratory, Bangkok, Thailand and Vietnam. Anopheles cracens Thailand. Anopheles dirus (Hainan strain, occurs southward from southern Thailand China) was obtained from the Department of through peninsular Malaysia (Perlis, Vector Ecology and Environment, Nagasaki Terengganu, Kuala Lipis Pahang states) into University, Japan. The species were identified Sumatra, Indonesia (Sallum et al., 2005; based on morphology (Rattanarithikul et al., Jiram et al., 2012). 2006; Somboon and Rattanarithikul, 2013) and Anopheles dirus and An. baimaii have the allele-specific polymerase chain reaction been incriminated as the principle vectors (AS-PCR) method of Walton et al. (1999). of the malarial protozoa Plasmodium Briefly, genomic DNA was extracted from falciparum and P. vivax in China and wings and legs of individual mosquitoes Southeast Asia (Manguin et al., 2008; using the PureLink® Genomic DNA Kit Saeung, 2012; Tainchum et al., 2015), while (Invitrogen, USA), according to the manu- An. cracens has been found to be the main facturer’s recommendations. Each PCR vector of P. knowlesi in peninsular Malaysia reaction was conducted using a 25 µl volume (Pahang) (Vythilingam et al., 2008; Jiram et containing 0.5 U of Taq DNA polymerase al., 2012). (Invitrogen, USA), 1x Taq buffer, 1.5 mM of Undoubtedly, correct identification of MgCl2, 0.2 mM of dNTP, 0.25 µM of each vector species is important for proper primer and 1 µl of the extracted DNA. The management and control of malaria. How- amplification profile consisted of an initial ever, identification of members of the Dirus denaturation at 94°C for 5 min, 35 cycles Complex is difficult due to overlapping at 94°C for 30 s, 53°C for 30 s, 72°C for 30 s morphological characters (Hii and Rueda, and a final extension at 72°C for 5 min. The 2013). Various methods for recognition and amplified products were electrophoresed confirmation of the taxonomic status of the on 1.5% agarose gel and stained with SYBR® individual species have been investigated, Safe DNA gel stain (Invitrogen, USA). including cytogenetics (Baimai, 1988; Baimai, 1998), enzyme electrophoresis Mosquito rearing (Green et al., 1992) and molecular genetics A colony of each of the three strains was (Walton et al., 1999; Sallum et al., 2005; established and maintained in an insectary Phunngam et al., 2017). Furthermore, of the Department of Parasitology, Faculty Somboon et al. (2009) investigated the of Medicine, Chiang Mai University, using structure of the cibarial armature for the procedures described by Choochote and distinguishing four species of the Dirus Saeung (2013). The insectary was maintained Complex but no significant differences were at 27±2°C, 70–80% relative humidity and observed. However, the antennal sensilla illuminated by a combination of natural of members of the complex have not been daylight from a glass window and fluorescent investigated. In the present study, the various lighting provided for approximately 12 h a types of sensilla borne on the antennae of day. females of An. dirus and An. cracens were examined using scanning electron micro- Light microscopy scopy, and are described here for the first Large sensilla coeloconica (lco) on each time. antennal flagellum of five-day-old female 927 mosquitoes were observed using an Olympus sputter-coated with gold. Sensilla were BX53 compound microscope. Individual observed and photographed in a JEOL- specimens were immersed in 10% potassium JSM6610LV scanning electron microscope. hydroxide (KOH) solution in a small bottle and held in an oven at 45°C for 30–45 min. Statistical analysis After clearing, they were washed with 80% The number of large sensilla coeloconica on ethanol, their antennae were removed the antennae of specimens of An. cracens using an insect needle and the two antennae and the two strains of An. dirus were of each female were mounted together on analyzed using the Kruskal-Wallis test. A a microscope slide with Neo-shigaral post-hoc Dunn’s test was used for multiple medium (Tokyo, Japan). The large sensilla comparisons of means. All data were coeloconica borne on the left and right analyzed using IBM SPSS statistics, version flagellum of 30 females of each strain were 24 for Windows (SPSS Inc., Chicago). The counted (n = 60 flagella/strain) (Taai et al., level of significance was set at 5% (p-value 2017). < 0.05). Scanning electron microscopy Thirty heads of four- to five-day-old females RESULTS of each strain were removed under a stereomicroscope and rinsed three times in Molecular identification phosphate buffer (pH 7.4) to remove surface The AS-PCR confirmed the morphological debris. The heads were then dehydrated identification of An. dirus (Thailand and through an ethanol series of 35, 70, 80 (10 Hainan strains) and An. cracens. PCR min, two changes) and 95% (15 min, two species-specific products were 562 bp and changes), followed by absolute ethanol 514 bp for An. dirus (both strains) and (10 min, two changes), and then dried in a An. cracens, respectively (Figure 1). critical point dryer. The antennae were carefully dissected from the head capsule Morphology of antennal sensilla under a stereomicroscope, as described by In general, the antennae of female mosquitoes Hempolchom et al. (2017). The antennae consist of two basal segments (scape and were mounted on aluminum stubs with pedicel) and an elongate segmented double-sided carbon adhesive tape and flagellum (Figures 2A–2C). The scape is the Figure 1. Gel of allele-specific PCR for distinguishing An. dirus and An. cracens. Lanes 1 and 2: An. dirus, Thailand strain (562 bp); lanes 3 and 4: An. dirus, Hainan strain (562 bp); lanes 5 and 6: An. cracens, Thailand strain (514 bp); lane M: 100 bp ladder. 928 Figure 2. Scanning electron micrographs of the antenna of females of An. dirus (virtually identical in An. cracens). (A) The flagellum consisting of 13 flagellomeres. (B) The scape (Sc), pedicel (Pe) and first flagellomere (I), densely covered with aculeae (ac). (C) The basal plate (Bpl) of flagellomere I connected with the pedicel.
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